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Ann Thorac Surg 2006;81:1963-1968
© 2006 The Society of Thoracic Surgeons

Original article: General thoracic

Gemcitabine-Cisplatin Chemotherapy Before Lung Resection: A Case-Matched Analysis of Early Outcome

Alessandro Brunelli, MD * , Francesco Xiume', MD, Majed Al Refai, MD, Michele Salati, MD, Rita Marasco, MD, Armando Sabbatini, MD

Unit of Thoracic Surgery, "Umberto I" Regional Hospital, Ancona, Italy

Accepted for publication January 3, 2006.

* Address correspondence to Dr Brunelli, Via S. Margherita 23, Ancona 60129, Italy (Email: alexit_2000{at}yahoo.com).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
BACKGROUND: The objective of the present study was to assess whether neoadjuvant chemotherapy with gemcitabine and cisplatin was associated with an increased incidence of morbidity and mortality after major lung resection for lung cancer.

METHODS: We analyzed 570 patients who underwent lobectomy or pneumonectomy for nonsmall-cell lung cancer at our institution from January 2000 through June 2005. Of these, 70 patients underwent three cycles of gemcitabine-cisplatin chemotherapy before operation for locally advanced disease. Propensity scores were constructed to match those patients undergoing neoadjuvant chemotherapy and lung resection with those undergoing surgery alone. The propensity score analysis yielded two groups of 70 well-matched pairs that were compared in terms of baseline characteristics and early outcome (morbidity, mortality, length of postoperative stay, intensive care unit admission).

RESULTS: The two case-matched groups had similar morbidity (p = 0.8), mortality (p = 0.4), perioperative blood transfusions (p = 0.8) and intensive care unit admission rates (p = 0.8). Likewise, the length of postoperative stay did not differ between the groups (p = 0.9).

CONCLUSIONS: Gemcitabin-cisplatin neoadjuvant chemotherapy appears to be safe before major lung resection. This finding warrants its use for efficacy studies of locally advanced and even early-stage lung cancer.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Neoadjuvant chemotherapy before operation has become a widely used approach for locally advanced nonsmall-cell lunger cancer (NSCLC) [1–4], and has been recently proposed even for the early stages of the disease [4, 5]. In this regard, the combination of gemcitabine and cisplatin has been shown to be an effective and tolerable regimen in recent phase II studies [6–10]. However, the widespread use of the induction treatment before lung resection should be warranted only in case the benefits gained in terms of long-term prognosis would not be offset by a potential increase in early morbidity and mortality.

This subject has been investigated in previous analyses with variable results [4, 11–16]. Most of these studies were retrospective and comprised heterogeneous groups of patients, including even lesser resections (wedge and segmentectomy) and multiple different chemotherapy protocols. Furthermore, they were usually based on old series dating back, in most cases, even more than a decade, with inherent modifications of treatment schedules and selection criteria [11–16], and generally lacked a case-matched control group selected by balancing scores (such as propensity score). The few prospective studies published to date [1–4] did not evaluate early postoperative morbidity, and the patients were not randomized based on important risk factors such as carbon monoxide lung diffusion capacity and exercise tolerance, which may have had influenced the early outcome. Finally, gemcitabine-cisplatin doublet was used only in a small percentage of patients (less than 20% in each study) in just two series [13, 14].

The aim of the present study was to compare the early outcome of a recent series (from 2000 through June 2005) of patients undergoing major lung resection after gemcitabine-cisplatin neoadjuvant chemotherapy for locally advanced lung cancer, with that of propensity score case-matched controls undergoing major lung resection without neoadjuvant chemotherapy.


   Patients and Methods
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 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
We analyzed 570 patients (449 male, 121 female) undergoing major lung resection (478 lobectomy/bilobectomy, 92 pneumonectomy) for NSCLC from January 2000 through June 2005 at our institution. The study was approved by the local Institutional Review Board after informed consent was obtained from all patients. This is an observational study performed on a prospective, quality-controlled, electronic database.

Criteria of resectability were assessed by computed tomography (CT) scan, bronchoscopy, and whenever indicated, mediastinal staging procedures (cervical mediastinoscopy, fine-needle aspiration through bronchoscopy, or video-assisted thoracoscopy). Operability was evaluated by pulmonary function tests, extensive cardiologic evaluation, and exercise testing (stair-climbing test and cycle-ergospirometry). Patients with a predicted postoperative forced expiratory volume in 1 second (FEV1) and predicted postoperative carbon monoxide diffusion lung capacity (DLCO) less than 30% in association with a poor exercise tolerance (height at stair-climbing test less than 12 m [12] or maximum oxygen consumption (VO2max) less than 10 mL · kg-1 · min-1) were deemed inoperable. During the period of this study, only 4 patients were excluded from operation owing to insufficient cardiopulmonary reserve (none after neoadjuvant chemotherapy).

Seventy patients (12%) underwent lung resection for a locally advanced NSCLC stage (N2 or T4 at preoperative staging) after neoadjuvant chemotherapy, consisting of three cycles (each cycle every 3 weeks) of gemcitabine plus cisplatin. An additional 9 patients had concurrent chemoradiotherapy, and for the sake of homogeneity, they were excluded from the propensity matching analysis. The operation was performed approximately after 1 month from completion of chemotherapy in all patients. The criterion for resectability after chemotherapy was responding or stable disease, as evaluated by clinical restaging.

Four certified thoracic surgeons performed all the operations through a muscle-sparing lateral thoracotomy. In patients undergoing pneumonectomy after chemotherapy, the bronchial stump was always buttressed with viable tissue (intercostal muscle flap or pericardial fat pad). Postoperative treatment was standardized and focused on thoracotomy chest pain control, chest physiotherapy, early mobilization, and antithrombotic and antibiotic prophylaxis.

Statistical Analysis
Selection bias was addressed by constructing propensity scores [18, 19]. The aim of the analysis was to match patients who were undergoing neoadjuvant chemotherapy before lung resection with those who were not, according to baseline characteristics, and compare surgical outcomes (morbidity, mortality, length of postoperative stay, intensive care unit admission) between the matched groups. Before matching patients, a parsimonious explanatory model was developed by bootstrap bagging for variables selection [20]. The probability of undergoing neoadjuvant chemotherapy (propensity score) was estimated by logistic regression analysis incorporating the variables identified in the parsimonious model (whose stability was assessed by bootstrap analysis) plus additional baseline variables. Therefore, the variables used in the model were the following: age, sex, body mass index, type of operation (lobectomy versus pneumonectomy), extension of resection (extended versus nonextended), FEV1, forced vital capacity (FVC), FEV1/FVC ratio, DLCO, total lung capacity, residual volume, arterial carbon dioxide and oxygen tensions, preoperative hemoglobin level, presence of a concomitant cardiac disease, Charlson Comorbidity Index (CCI) [21], smoking history (pack-years), percentage of functioning lung parenchyma removed during operation (Func loss%), height reached at the preoperative symptom-limited stair-climbing test, and VO2max (mL · kg-1 · min-1) calculated from the stair-climbing test (see Appendix for explanation of variables). The choice to perform neoadjuvant chemotherapy was initially based on the presence of cN2 or cT4 stages, and patients with earlier stage disease were undergoing surgery alone. Because of this necessary imbalance, clinical staging was not used in the construction of the propensity model. The distribution of the final pathologic T and N stages in the two groups is shown in Table 1.


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  		Table 1. Final Pathologic pT and pN Stages in the Two Propensity Score Matched Groups (70 Pairs)
 
The method of generating a parsimonious model and then augmenting it with other factors to develop the propensity model was described elsewhere [19]. As stated by its developers [22], the propensity model is not parsimonious. In fact, the goal is to balance patient characteristics by incorporating "everything" recorded that may relate to either systematic bias or simply bad luck that has otherwise unbalanced the comparison groups of interest, ignoring usual concerns about model overdetermination [19, 23]. The c-index, or area under the receiver operator curve (ROC), for this model was 0.82. All variables were at least 95% complete, and sporadic missing values were imputed by taking the most frequent response category or averaging nonmissing values for continuous variables. Greedy matching techniques were then used to select stair-climbing counterparts to the non–stair-climbing patients by choosing the patient with the nearest propensity score [19].

The procedure yielded 70 well-matched pairs. The following operations were performed in the two groups: in the neoadjuvant chemotherapy group, 12 right upper lobectomies, 10 left upper lobectomies, 5 left lower lobectomies, 4 upper bilobectomies, 4 lower bilobectomies, 3 right lower lobectomies, 2 middle lobectomies, 19 left pneumonectomies, and 11 right pneumonectomies; in the surgery alone group, 8 left lower lobectomies, 8 lower bilobectomies, 7 right lower lobectomies, 6 left upper lobectomies, 4 right upper lobectomies, 3 upper bilobectomies, 2 middle lobectomies, 22 right pneumonectomies, and 10 left pneumonectomies. The two groups of propensity score matched patients were compared by using the {chi}2 test or the Fisher's exact test for categorical variables, and the unpaired Student's t test or the Mann-Whitney U test for continuous ones.

All statistical tests were two-tailed, and a significance level of p less than 0.05 was selected.

The analyses were performed by using the Stata 8.2 (Stata Corp, College Station, Texas) statistical software.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Total morbidity and mortality rates were 24% (138 cases) and 4.4% (25 cases), respectively. Among the 70 patients undergoing gemcitabine-cisplatin chemotherapy before lung resection, the morbidity and mortality rates were of 26% (18 cases) and 2.9% (2 cases), respectively. Thirty patients underwent neoadjuvant chemotherapy and pneumonectomy. Their morbidity and mortality rates were 30% (9 cases) and 0, respectively. Among the 9 patients with concurrent chemoradiotherapy (not included in the case-matching analysis), there was only 1 cardiopulmonary complication and no deaths.

Propensity score analysis yielded 70 well-matched pairs of patients with and without neoadjuvant chemotherapy before lung resection (Table 2).


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  		Table 2. Results of Comparison of Baseline Characteristics Between Propensity Score Matched Groups (70 Pairs)
 
Table 3 shows the results of the comparison of outcome between the two propensity score matched groups of patients. No significant differences were noted in terms of morbidity, mortality, intensive care unit admission rates, and perioperative blood transfusions between the two groups. Length of postoperative stay was also similar between the groups.


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  		Table 3. Results of Comparison of Outcome Between Propensity Score Matched Groups (70 Pairs)
 
Table 4 shows a breakdown of the types of complications in the two case-matched groups.


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  		Table 4. Breakdown of Cardiopulmonary Complications in the Two Matched Groups (70 Pairs)
 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
The present study showed that gemcitabine-cisplatin neoadjuvant chemotherapy did not increase the incidence of morbidity nor mortality nor intensive care unit admission rates after major lung resection, compared with propensity score matched patients who underwent surgery without chemotherapy.

Some authors reported an increased incidence of morbidity and mortality after neoadjuvant chemotherapy and lung resection, particularly after pneumonectomy, with mortality rates as high as 24% [4, 11, 12, 15]. We did not notice this association. Even after pneumonectomy, the morbidity and mortality rates were low, confirming other studies that did not find neoadjuvant chemotherapy to increase the operative risk [13, 14, 16].

The main problems with most of the published analyses are that they were based on old series, comprising heterogeneous groups of patients in terms of operation performed (including also wedge resections and segmentectomies) and chemotherapy agents used, and lacked matched controls selected by balancing scores, through which important risk factors potentially associated with morbidity and mortality can be controlled. In particular, the gemcitabine-cisplatin combination has never been specifically assessed in terms of postoperative early outcome in case-matched comparisons. This form of treatment has shown promising results in terms of efficacy and tolerability in a number of phase II trials [6–10], and multiple phase III projects are currently underway to assess its role even in the early stages of NSCLC (GINEST [Gemcitabine in Neoadjuvant Early Stage Therapy] and CHEST [Chemotherapy for Early Stages Trial] protocols, presented at the recent American Society of Clinical Oncology meeting).

It was the aim of this study to assess the influence of this form of induction treatment on morbidity and mortality after major lung resection. To this purpose, we based our analysis on a recent series (starting from 2000) of patients undergoing major lung resections after gemcitabine plus cisplatin chemotherapy who were compared with case-matched counterparts (treated by surgery alone) selected by propensity score analysis.

Even though efficacy studies on neoadjuvant chemotherapy are few and have reported controversial results [1–4], a combined modality treatment for potentially resectable locally advanced lung cancer is a widely accepted approach. It is generally believed that patients with stage III lung cancer would benefit from preoperative chemotherapy [24]. In this setting, the construction of prospective randomized trials bears important clinical and ethical issues. In this regard, propensity score case-matched analysis [18, 19] is considered the most rigorous method available for the so-called "apples-to-apples" investigation of causal effects on outcome in a nonrandomized setting [25]. Because associations found through traditional multivariable regression may be misleading because of underrepresentation of one covariate of interest within levels of another, propensity scores are recommended to adjust for confounding background characteristics [25].

In this study, a number of baseline and operative characteristics that may have had a potential impact on postoperative outcome were used to match the patients, including exercise tolerance and carbon monoxide lung diffusion capacity. In particular, this latter characteristic has been shown to be negatively affected by gemcitabine-cisplatin chemotherapy and to influence surgical morbidity after lung resection [26, 27]. The inclusion of exercise tolerance and DLCO among the variables used for patients matching increases the reliability of the results of the comparison between the groups.

Nevertheless, this study has potential limitations. First, this is not a randomized trial, and even though the propensity score analysis constitutes the most rigorous method for investigating the causal effects in this setting, it cannot completely account for unknown variables affecting the outcome that are not correlated strongly with the measured variables. Therefore, the results generated by this analysis cannot be interpreted as definitive.

Second, being an observational study performed at a tertiary referral center with patients treated with "ad hoc" chemotherapy protocols and referred from a number of local regional hospitals, it was not possible to retrieve detailed information about schedules, patients' compliance, and complications related to chemotherapy.

In conclusion, we showed that gemcitabine-cisplatin neoadjuvant chemotherapy for potentially resectable locally advanced NSCLC did not increase early morbidity and mortality after major lung resection compared with case-matched patients treated by surgery alone. The safety of this drug combination demonstrated by our results warrants the implementation of efficacy studies, for locally advanced and early stages of NSCLC.


   Appendix
 
Preoperative and Operative Variables
For the purpose of the present study the following spirometric variables were considered: forced expiratory volume in 1 second (FEV1); forced vital capacity (FVC); FEV1/FVC ratio; carbon monoxide diffusion lung capacity (DLCO); residual volume; total lung capacity; predicted postoperative FEV1 (ppoFEV1) calculated by the formula, (preoperative FEV1/number of preoperative functioning segments) x number of postoperative functioning segments; predicted postoperative DLCO (ppoDLCO) calculated by the formula (preoperative DLCO/number of preoperative functioning segments) x number of postoperative functioning segments.

Pulmonary function tests were performed according to the American Thoracic Society criteria. The DLCO was measured by the single-breath method. Results of spirometry were collected after bronchodilator administration and were expressed as percentage of predicted for age, sex, and height, with the exception of the FEV1/FVC ratio.

The number of functioning segments was estimated by means of computed tomography scan and bronchoscopy findings. In patients with a calculated ppoFEV1 less than 50% of predicted and in all pneumonectomy candidates, a quantitative perfusion lung scan was used, according to Markos and associates [28].

For the purpose of the present study, a concomitant cardiac disease (cardiac comorbidity) was defined as follows: previous cardiac surgery, previous myocardial infarction, history of coronary artery disease, current treatment for hypertension, arrhythmia, or cardiac failure.

An extended resection was defined as a lung resection associated with resection of chest wall, diaphragm, pericardium, other mediastinal tissue, or extrapleural resections.

The following additional variables were used for comparison of patients with and without neoadjuvant chemotherapy: age, sex, body mass index; type of operation (lobectomy versus pneumonectomy), arterial carbon dioxide level (PaCO2), arterial oxygen tension (PaO2), preoperative hemoglobin level, concomitant cardiac disease, operation time, percentage of functional parenchyma removed during operation (Func loss%), smoking history (pack-years), Charlson comorbidity index (CCI); height reached at the preoperative symptom-limited stair-climbing test (m); maximum oxygen consumption calculated from the performance at the stair-climbing test (VO2max, mL · kg-1 · min-1). The CCI is a comorbidity index that was shown to predict postoperative complications after lung resection [21]. We computed the number of pack-years of smoking as the total number of years smoked, times the average number of cigarettes smoked per day, divided by 20. The stair-climbing test [17] was performed within a week from the operation on room air for all patients. Our hospital has 16 flights of stairs, each flight having 11 steps. Each step is 0.155 m in height. The patients were asked to climb, at a pace of their own choice, the maximum number of steps and to stop only for exhaustion, limiting dyspnea, leg fatigue, or chest pain.. For each patient, the number of steps climbed and the time taken to complete the test was recorded. The following ergometric variables were calculated: work (height of the step in meters X steps per minute x body weight in kilograms x 0.1635) [29]; maximum oxygen consumption (VO2max) in milliters per minute (5.8 x body weight in kilograms + 151 + 10.1 x work) [29].

Outcome Variables
Postoperative cardiopulmonary complications and mortality were considered as those occurring within 30 days from operation or during a longer period if the patient was still in the hospital. For the sake of comparison with other authors [30] and according to the European Thoracic Database [31], the following cardiopulmonary complications were included: respiratory failure requiring mechanical ventilation for more than 48 hours; pneumonia; atelectasis requiring bronchoscopy; pulmonary edema; pulmonary embolism; myocardial infarction; hemodynamically unstable arrhythmia requiring medical treatment; cardiac failure; stroke; acute renal insufficiency.

Other endpoints were evaluated, such as the number of perioperative blood units transfused perioperatively, the emergency intensive care unit admission after initial recovery from the operation, the length of postoperative stay, and additional complications (bronchopleural fistula, empyema, air leak longer than 7 days).


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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